Bias-free estimation of information content in temporally sparse neuronal activity

Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterp...

Celý popis

Uložené v:
Podrobná bibliografia
Vydané v:PLoS computational biology Ročník 18; číslo 2; s. e1009832
Hlavní autori: Sheintuch, Liron, Rubin, Alon, Ziv, Yaniv
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Public Library of Science 01.02.2022
Public Library of Science (PLoS)
Predmet:
ISSN:1553-7358, 1553-734X, 1553-7358
On-line prístup:Získať plný text
Tagy: Pridať tag
Žiadne tagy, Buďte prvý, kto otaguje tento záznam!
Abstract Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterpretation of coding characteristics. This bias is exacerbated in Ca 2+ imaging because of the temporal sparsity of elevated Ca 2+ signals. Here, we introduce methods to correct for the bias in the naïve estimation of information content from limited sample sizes and temporally sparse neuronal activity. We demonstrate the higher accuracy of our methods over previous ones, when applied to Ca 2+ imaging data recorded from the mouse hippocampus and primary visual cortex, as well as to simulated data with matching tuning properties and firing statistics. Our bias-correction methods allowed an accurate estimation of the information place cells carry about the animal’s position ( spatial information ) and uncovered the spatial resolution of hippocampal coding. Furthermore, using our methods, we found that cells with higher peak firing rates carry higher spatial information per spike and exposed differences between distinct hippocampal subfields in the long-term evolution of the spatial code. These results could be masked by the bias when applying the commonly used naïve calculation of information content. Thus, a bias-free estimation of information content can uncover otherwise overlooked properties of the neural code.
AbstractList Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterpretation of coding characteristics. This bias is exacerbated in Ca2+ imaging because of the temporal sparsity of elevated Ca2+ signals. Here, we introduce methods to correct for the bias in the naïve estimation of information content from limited sample sizes and temporally sparse neuronal activity. We demonstrate the higher accuracy of our methods over previous ones, when applied to Ca2+ imaging data recorded from the mouse hippocampus and primary visual cortex, as well as to simulated data with matching tuning properties and firing statistics. Our bias-correction methods allowed an accurate estimation of the information place cells carry about the animal's position (spatial information) and uncovered the spatial resolution of hippocampal coding. Furthermore, using our methods, we found that cells with higher peak firing rates carry higher spatial information per spike and exposed differences between distinct hippocampal subfields in the long-term evolution of the spatial code. These results could be masked by the bias when applying the commonly used naïve calculation of information content. Thus, a bias-free estimation of information content can uncover otherwise overlooked properties of the neural code.
Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterpretation of coding characteristics. This bias is exacerbated in Ca2+ imaging because of the temporal sparsity of elevated Ca2+ signals. Here, we introduce methods to correct for the bias in the naïve estimation of information content from limited sample sizes and temporally sparse neuronal activity. We demonstrate the higher accuracy of our methods over previous ones, when applied to Ca2+ imaging data recorded from the mouse hippocampus and primary visual cortex, as well as to simulated data with matching tuning properties and firing statistics. Our bias-correction methods allowed an accurate estimation of the information place cells carry about the animal’s position (spatial information) and uncovered the spatial resolution of hippocampal coding. Furthermore, using our methods, we found that cells with higher peak firing rates carry higher spatial information per spike and exposed differences between distinct hippocampal subfields in the long-term evolution of the spatial code. These results could be masked by the bias when applying the commonly used naïve calculation of information content. Thus, a bias-free estimation of information content can uncover otherwise overlooked properties of the neural code. Neuroscientists interested in understanding the nature of the neural code often apply methods derived from the mathematical framework of information theory to quantify the statistical relationship between neuronal activity and a certain variable of interest. For instance, when studying the neural basis for spatial navigation, it is useful to estimate how much information hippocampal neurons carry about the position of an animal within a specific environment. However, the standard measures for estimating information content suffer from an upward bias when applied to small sample sizes, which may lead to misinterpretation of the data. This bias is more pronounced in data from calcium imaging–a widely used technique for recording neuronal activity–because the activity extracted from the measured calcium signal is sparse in time. In this work, we introduce new methods to correct the bias in the naïve estimation of information content from limited sample sizes and such temporally sparse neuronal activity. We show that our bias-correction methods allow an accurate estimation of the information content carried by the activity obtained from calcium imaging data in both hippocampal and cortical neurons, and help uncover differences in the way information content changes during learning across neural circuits.
Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterpretation of coding characteristics. This bias is exacerbated in Ca2+ imaging because of the temporal sparsity of elevated Ca2+ signals. Here, we introduce methods to correct for the bias in the naïve estimation of information content from limited sample sizes and temporally sparse neuronal activity. We demonstrate the higher accuracy of our methods over previous ones, when applied to Ca2+ imaging data recorded from the mouse hippocampus and primary visual cortex, as well as to simulated data with matching tuning properties and firing statistics. Our bias-correction methods allowed an accurate estimation of the information place cells carry about the animal's position (spatial information) and uncovered the spatial resolution of hippocampal coding. Furthermore, using our methods, we found that cells with higher peak firing rates carry higher spatial information per spike and exposed differences between distinct hippocampal subfields in the long-term evolution of the spatial code. These results could be masked by the bias when applying the commonly used naïve calculation of information content. Thus, a bias-free estimation of information content can uncover otherwise overlooked properties of the neural code.Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterpretation of coding characteristics. This bias is exacerbated in Ca2+ imaging because of the temporal sparsity of elevated Ca2+ signals. Here, we introduce methods to correct for the bias in the naïve estimation of information content from limited sample sizes and temporally sparse neuronal activity. We demonstrate the higher accuracy of our methods over previous ones, when applied to Ca2+ imaging data recorded from the mouse hippocampus and primary visual cortex, as well as to simulated data with matching tuning properties and firing statistics. Our bias-correction methods allowed an accurate estimation of the information place cells carry about the animal's position (spatial information) and uncovered the spatial resolution of hippocampal coding. Furthermore, using our methods, we found that cells with higher peak firing rates carry higher spatial information per spike and exposed differences between distinct hippocampal subfields in the long-term evolution of the spatial code. These results could be masked by the bias when applying the commonly used naïve calculation of information content. Thus, a bias-free estimation of information content can uncover otherwise overlooked properties of the neural code.
Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterpretation of coding characteristics. This bias is exacerbated in Ca 2+ imaging because of the temporal sparsity of elevated Ca 2+ signals. Here, we introduce methods to correct for the bias in the naïve estimation of information content from limited sample sizes and temporally sparse neuronal activity. We demonstrate the higher accuracy of our methods over previous ones, when applied to Ca 2+ imaging data recorded from the mouse hippocampus and primary visual cortex, as well as to simulated data with matching tuning properties and firing statistics. Our bias-correction methods allowed an accurate estimation of the information place cells carry about the animal’s position ( spatial information ) and uncovered the spatial resolution of hippocampal coding. Furthermore, using our methods, we found that cells with higher peak firing rates carry higher spatial information per spike and exposed differences between distinct hippocampal subfields in the long-term evolution of the spatial code. These results could be masked by the bias when applying the commonly used naïve calculation of information content. Thus, a bias-free estimation of information content can uncover otherwise overlooked properties of the neural code.
Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is limited, a naïve estimation of the information content typically contains a systematic overestimation (upward bias), which may lead to misinterpretation of coding characteristics. This bias is exacerbated in Ca.sup.2+ imaging because of the temporal sparsity of elevated Ca.sup.2+ signals. Here, we introduce methods to correct for the bias in the naïve estimation of information content from limited sample sizes and temporally sparse neuronal activity. We demonstrate the higher accuracy of our methods over previous ones, when applied to Ca.sup.2+ imaging data recorded from the mouse hippocampus and primary visual cortex, as well as to simulated data with matching tuning properties and firing statistics. Our bias-correction methods allowed an accurate estimation of the information place cells carry about the animal's position (spatial information) and uncovered the spatial resolution of hippocampal coding. Furthermore, using our methods, we found that cells with higher peak firing rates carry higher spatial information per spike and exposed differences between distinct hippocampal subfields in the long-term evolution of the spatial code. These results could be masked by the bias when applying the commonly used naïve calculation of information content. Thus, a bias-free estimation of information content can uncover otherwise overlooked properties of the neural code.
Audience Academic
Author Sheintuch, Liron
Rubin, Alon
Ziv, Yaniv
AuthorAffiliation University Medical Center Hamburg-Eppendorf Center for Molecular Neurobiology Hamburg: Universitatsklinikum Hamburg-Eppendorf Zentrum fur Molekulare Neurobiologie Hamburg, GERMANY
Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel
AuthorAffiliation_xml – name: University Medical Center Hamburg-Eppendorf Center for Molecular Neurobiology Hamburg: Universitatsklinikum Hamburg-Eppendorf Zentrum fur Molekulare Neurobiologie Hamburg, GERMANY
– name: Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel
Author_xml – sequence: 1
  givenname: Liron
  orcidid: 0000-0003-4245-5786
  surname: Sheintuch
  fullname: Sheintuch, Liron
– sequence: 2
  givenname: Alon
  surname: Rubin
  fullname: Rubin, Alon
– sequence: 3
  givenname: Yaniv
  orcidid: 0000-0001-6658-9303
  surname: Ziv
  fullname: Ziv, Yaniv
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35148310$$D View this record in MEDLINE/PubMed
BookMark eNqVUttu1DAQtVARvcAfIIjECzxk8SV2Eh6QSsVlpQqkAs-W49iLV9k4tZ2K_Xsmu2nVrRASykMmk3POzJyZU3TU-94g9JzgBWElebv2Y-hVtxh04xYE47pi9BE6IZyzvGS8OroXH6PTGNcYQ1iLJ-iYcVJUjOATdPXBqZjbYExmYnIblZzvM28z11sf5k_t-2T6BLksmc3gg-q6bRYHFaLJejMGD41kSid349L2KXpsVRfNs_l9hn5--vjj4kt--e3z8uL8MteCsZQbawQmVLHKGlI3raUEtwW1VDVUQ1TWjBZtTZpKNSWxwpJSqdZgoRlvBavYGXq51x06H-VsR5RUFCCLoQYglntE69VaDgHGC1vplZO7hA8rqUJyujOScC1wgTmmnBcN0zVroAnKdNUwy9Wk9X6uNjYb02rwA2w4ED3807tfcuVvZFUxwcpJ4PUsEPz1CGbLjYvadJ3qjR-nvmlFa86KAqCvHkD_Pt1ij1opGGDaF9TV8LRm42BlxjrIn4uaFwIok-ybA8Jurb_TSo0xyuX3q__Afj3EvrhvzZ0nt1cGgGIP0MHHGIy9gxAsp2O-nU9OxyznYwbauwc07dLuImFQ1_2b_Ad3SPwo
CitedBy_id crossref_primary_10_1016_j_isci_2025_112489
crossref_primary_10_1038_s41467_023_41803_8
crossref_primary_10_7554_eLife_90069_3
crossref_primary_10_1016_j_neuron_2023_05_014
crossref_primary_10_7554_eLife_90069
crossref_primary_10_1007_s10827_025_00901_w
Cites_doi 10.1523/JNEUROSCI.1537-13.2013
10.1162/neco.2007.19.11.2913
10.1098/rspb.1999.0736
10.1523/JNEUROSCI.17-23-09315.1997
10.1038/ncomms13805
10.1371/journal.pcbi.1008927
10.1038/s41586-018-0516-1
10.1523/JNEUROSCI.5393-12.2014
10.1523/JNEUROSCI.3824-08.2008
10.1523/JNEUROSCI.1788-20.2020
10.1038/nature04701
10.1038/s41593-019-0550-9
10.1002/hipo.450040404
10.1126/science.1188210
10.1523/JNEUROSCI.4261-08.2008
10.1162/089976698300017115
10.7554/eLife.28728
10.1016/j.neuron.2005.03.026
10.1162/08997660252741176
10.1007/BF00216963
10.1016/j.neuron.2020.05.022
10.1080/0954898X.1996.11978656
10.1088/0954-898X_7_2_018
10.1016/S0896-6273(03)00165-X
10.1523/JNEUROSCI.23-37-11539.2003
10.1016/j.neuron.2017.03.004
10.1523/JNEUROSCI.1704-07.2007
10.1152/jn.1987.57.1.162
10.1016/j.neuron.2015.07.007
10.1038/nm.2292
10.1016/j.neuron.2015.11.037
10.1016/j.celrep.2017.10.013
10.1126/science.1188224
10.1162/neco.1995.7.2.399
10.1016/j.cub.2020.02.018
10.1126/science.aat5397
10.7554/eLife.12247
10.1016/S0896-6273(00)81205-2
10.1016/j.neuroscience.2018.01.066
10.1038/nature12354
10.1103/PhysRevLett.80.197
10.1038/nn.3329
10.1016/j.neuron.2014.12.001
10.1523/JNEUROSCI.18-21-09020.1998
10.1152/jn.00559.2007
10.1126/science.1151120
10.1038/nmeth.1694
10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K
10.1162/089976603321780272
10.1037/h0026857
ContentType Journal Article
Copyright COPYRIGHT 2022 Public Library of Science
2022 Sheintuch et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2022 Sheintuch et al 2022 Sheintuch et al
Copyright_xml – notice: COPYRIGHT 2022 Public Library of Science
– notice: 2022 Sheintuch et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2022 Sheintuch et al 2022 Sheintuch et al
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
ISN
ISR
3V.
7QO
7QP
7TK
7TM
7X7
7XB
88E
8AL
8FD
8FE
8FG
8FH
8FI
8FJ
8FK
ABUWG
AEUYN
AFKRA
ARAPS
AZQEC
BBNVY
BENPR
BGLVJ
BHPHI
CCPQU
DWQXO
FR3
FYUFA
GHDGH
GNUQQ
HCIFZ
JQ2
K7-
K9.
LK8
M0N
M0S
M1P
M7P
P5Z
P62
P64
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
Q9U
RC3
7X8
5PM
DOA
DOI 10.1371/journal.pcbi.1009832
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Gale In Context: Canada
Gale In Context: Science
ProQuest Central (Corporate)
Biotechnology Research Abstracts
Calcium & Calcified Tissue Abstracts
Neurosciences Abstracts
Nucleic Acids Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Computing Database (Alumni Edition)
Technology Research Database
ProQuest SciTech Collection
ProQuest Technology Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest One Sustainability
ProQuest Central UK/Ireland
Advanced Technologies & Computer Science Collection
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
ProQuest Technology Collection
Natural Science Collection
ProQuest One Community College
ProQuest Central Korea
Engineering Research Database
Proquest Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
SciTech Premium Collection
ProQuest Computer Science Collection
Computer Science Database
ProQuest Health & Medical Complete (Alumni)
ProQuest Biological Science Collection
Computing Database
ProQuest Health & Medical Collection
Medical Database
Biological Science Database
Advanced Technologies & Aerospace Database
ProQuest Advanced Technologies & Aerospace Collection
Biotechnology and BioEngineering Abstracts
ProQuest Central Premium
ProQuest One Academic
Publicly Available Content Database
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic (retired)
ProQuest One Academic UKI Edition
ProQuest Central China
ProQuest Central Basic
Genetics Abstracts
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
Computer Science Database
ProQuest Central Student
ProQuest Advanced Technologies & Aerospace Collection
ProQuest Central Essentials
ProQuest Computer Science Collection
Nucleic Acids Abstracts
SciTech Premium Collection
ProQuest Central China
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
Health Research Premium Collection
Natural Science Collection
Health & Medical Research Collection
Biological Science Collection
ProQuest Central (New)
ProQuest Medical Library (Alumni)
Advanced Technologies & Aerospace Collection
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
ProQuest Technology Collection
Health Research Premium Collection (Alumni)
Biological Science Database
Neurosciences Abstracts
ProQuest Hospital Collection (Alumni)
Biotechnology and BioEngineering Abstracts
ProQuest Health & Medical Complete
ProQuest One Academic UKI Edition
Engineering Research Database
ProQuest One Academic
Calcium & Calcified Tissue Abstracts
ProQuest One Academic (New)
Technology Collection
Technology Research Database
ProQuest One Academic Middle East (New)
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central
ProQuest Health & Medical Research Collection
Genetics Abstracts
Biotechnology Research Abstracts
Health and Medicine Complete (Alumni Edition)
ProQuest Central Korea
ProQuest Computing
ProQuest Central Basic
ProQuest Computing (Alumni Edition)
ProQuest SciTech Collection
Advanced Technologies & Aerospace Database
ProQuest Medical Library
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList

Publicly Available Content Database
MEDLINE - Academic
CrossRef

MEDLINE

Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: PIMPY
  name: Publicly Available Content Database
  url: http://search.proquest.com/publiccontent
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
DocumentTitleAlternate Bias-free estimation of information content in temporally sparse neuronal activity
EISSN 1553-7358
ExternalDocumentID 2640120633
oai_doaj_org_article_15c6040502554b3c93bc0d23c8b3f5a3
PMC8836373
A695461204
35148310
10_1371_journal_pcbi_1009832
Genre Research Support, Non-U.S. Gov't
Journal Article
GeographicLocations Israel
GeographicLocations_xml – name: Israel
GrantInformation_xml – fundername: ;
– fundername: ;
  grantid: 2113/19
– fundername: ;
  grantid: ERC-CoG 101001226
GroupedDBID ---
123
29O
2WC
53G
5VS
7X7
88E
8FE
8FG
8FH
8FI
8FJ
AAFWJ
AAKPC
AAUCC
AAWOE
AAYXX
ABDBF
ABUWG
ACCTH
ACGFO
ACIHN
ACIWK
ACPRK
ACUHS
ADBBV
AEAQA
AENEX
AEUYN
AFFHD
AFKRA
AFPKN
AFRAH
AHMBA
ALMA_UNASSIGNED_HOLDINGS
AOIJS
ARAPS
AZQEC
B0M
BAIFH
BAWUL
BBNVY
BBTPI
BCNDV
BENPR
BGLVJ
BHPHI
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DWQXO
E3Z
EAP
EAS
EBD
EBS
EJD
EMK
EMOBN
ESX
F5P
FPL
FYUFA
GNUQQ
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IGS
INH
INR
ISN
ISR
ITC
J9A
K6V
K7-
KQ8
LK8
M1P
M48
M7P
O5R
O5S
OK1
OVT
P2P
P62
PHGZM
PHGZT
PIMPY
PJZUB
PPXIY
PQGLB
PQQKQ
PROAC
PSQYO
PV9
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
WOW
XSB
~8M
ADRAZ
ALIPV
C1A
CGR
CUY
CVF
ECM
EIF
H13
IPNFZ
NPM
RIG
WOQ
3V.
7QO
7QP
7TK
7TM
7XB
8AL
8FD
8FK
FR3
JQ2
K9.
M0N
P64
PKEHL
PQEST
PQUKI
PRINS
Q9U
RC3
7X8
PUEGO
5PM
-
AAPBV
ABPTK
ADACO
BBAFP
M~E
ID FETCH-LOGICAL-c633t-efe6012a38fe19bdf210d42f2ab2c0d479324d91b8ab71f6f17aade06c35d6383
IEDL.DBID DOA
ISICitedReferencesCount 8
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=001084614100003&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1553-7358
1553-734X
IngestDate Sun Apr 03 16:02:37 EDT 2022
Fri Oct 03 12:52:04 EDT 2025
Tue Nov 04 01:58:42 EST 2025
Thu Sep 04 16:34:17 EDT 2025
Sat Nov 29 14:47:38 EST 2025
Tue Nov 04 17:47:23 EST 2025
Thu Nov 13 15:48:08 EST 2025
Thu Nov 13 14:44:40 EST 2025
Mon Jul 21 05:45:45 EDT 2025
Sat Nov 29 06:12:38 EST 2025
Tue Nov 18 21:32:35 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 2
Language English
License This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Creative Commons Attribution License
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c633t-efe6012a38fe19bdf210d42f2ab2c0d479324d91b8ab71f6f17aade06c35d6383
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
The authors have declared that no competing interests exist.
ORCID 0000-0003-4245-5786
0000-0001-6658-9303
OpenAccessLink https://doaj.org/article/15c6040502554b3c93bc0d23c8b3f5a3
PMID 35148310
PQID 2640120633
PQPubID 1436340
ParticipantIDs plos_journals_2640120633
doaj_primary_oai_doaj_org_article_15c6040502554b3c93bc0d23c8b3f5a3
pubmedcentral_primary_oai_pubmedcentral_nih_gov_8836373
proquest_miscellaneous_2628295344
proquest_journals_2640120633
gale_infotracacademiconefile_A695461204
gale_incontextgauss_ISR_A695461204
gale_incontextgauss_ISN_A695461204
pubmed_primary_35148310
crossref_primary_10_1371_journal_pcbi_1009832
crossref_citationtrail_10_1371_journal_pcbi_1009832
PublicationCentury 2000
PublicationDate 2022-02-01
PublicationDateYYYYMMDD 2022-02-01
PublicationDate_xml – month: 02
  year: 2022
  text: 2022-02-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS computational biology
PublicationTitleAlternate PLoS Comput Biol
PublicationYear 2022
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References F Stefanini (pcbi.1009832.ref026) 2020; 107
JD Victor (pcbi.1009832.ref032) 2002; 66
A Rubin (pcbi.1009832.ref039) 2014; 34
TW Chen (pcbi.1009832.ref003) 2013; 499
SEJ de Vries (pcbi.1009832.ref042) 2020; 23
TJ Wills (pcbi.1009832.ref037) 2010; 328
N Brunel (pcbi.1009832.ref005) 1998; 10
S Panzeri (pcbi.1009832.ref016) 1996; 7
EJ Markus (pcbi.1009832.ref015) 1994; 4
RPJ Barretto (pcbi.1009832.ref058) 2011; 17
S Panzeri (pcbi.1009832.ref041) 1996; 7
S Panzeri (pcbi.1009832.ref056) 1999; 266
L Huang (pcbi.1009832.ref029) 2019
LM Optican (pcbi.1009832.ref009) 1987; 57
William E. Skaggs (pcbi.1009832.ref014) 1993
AB Saleem (pcbi.1009832.ref053) 2018; 562
Y Ziv (pcbi.1009832.ref001) 2013; 16
KK Ghosh (pcbi.1009832.ref002) 2011; 8
MP Karlsson (pcbi.1009832.ref044) 2008; 28
S Panzeri (pcbi.1009832.ref010) 2007; 98
JP Goodridge (pcbi.1009832.ref048) 1997; 17
L Rudelt (pcbi.1009832.ref040) 2021; 17
F Cacucci (pcbi.1009832.ref045) 2007; 27
M Bezzi (pcbi.1009832.ref027) 2002; 14
SK Rashid (pcbi.1009832.ref028) 2020
LM Optican (pcbi.1009832.ref012) 1991; 65
F. Rieke (pcbi.1009832.ref006) 1999
L Sheintuch (pcbi.1009832.ref019) 2020; 30
T Nakashiba (pcbi.1009832.ref023) 2008; 319
EA Mankin (pcbi.1009832.ref020) 2015; 85
A Treves (pcbi.1009832.ref011) 1995; 7
E Schneidman (pcbi.1009832.ref055) 2006; 440
A Dettner (pcbi.1009832.ref057) 2016; 7
IM Esteves (pcbi.1009832.ref025) 2021; 41
P Ledochowitsch (pcbi.1009832.ref047) 2019
BC Souza (pcbi.1009832.ref017) 2018; 375
SS Deshmukh (pcbi.1009832.ref022) 2011; 5
D Deitch (pcbi.1009832.ref043) 2021
XTA Allen (pcbi.1009832.ref051) 2016; 36
L. Paninski (pcbi.1009832.ref031) 2003; 15
P Zhou (pcbi.1009832.ref035) 2018; 7
A Rubin (pcbi.1009832.ref059) 2015; 4
I Nemenman (pcbi.1009832.ref034) 2002
CJ MacDonald (pcbi.1009832.ref050) 2013; 33
E Schneidman (pcbi.1009832.ref054) 2003; 23
SP Strong (pcbi.1009832.ref030) 1998; 80
L Lu (pcbi.1009832.ref018) 2015; 87
RF Langston (pcbi.1009832.ref038) 2010; 328
K Diba (pcbi.1009832.ref036) 2008; 28
L Sheintuch (pcbi.1009832.ref004) 2017; 21
KZ Tanaka (pcbi.1009832.ref024) 2018; 361
RW Stackman (pcbi.1009832.ref049) 1998; 18
JL Puchalla (pcbi.1009832.ref008) 2005; 46
WE Skaggs (pcbi.1009832.ref021) 1996; 6
N Brenner (pcbi.1009832.ref007) 2000; 26
MA Montemurro (pcbi.1009832.ref033) 2007; 19
EA Pnevmatikakis (pcbi.1009832.ref060) 2016; 89
GW Diehl (pcbi.1009832.ref052) 2017; 94
AG Carlton (pcbi.1009832.ref013) 1969; 71
K Nakazawa (pcbi.1009832.ref046) 2003; 38
References_xml – volume: 33
  start-page: 14607
  issue: 36
  year: 2013
  ident: pcbi.1009832.ref050
  article-title: Distinct Hippocampal Time Cell Sequences Represent Odor Memories in Immobilized Rats
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.1537-13.2013
– volume: 19
  start-page: 2913
  issue: 11
  year: 2007
  ident: pcbi.1009832.ref033
  article-title: Tight data-robust bounds to mutual information combining shuffling and model selection techniques.
  publication-title: Neural Comput.
  doi: 10.1162/neco.2007.19.11.2913
– volume: 266
  start-page: 1001
  issue: 1423
  year: 1999
  ident: pcbi.1009832.ref056
  article-title: Correlations and the encoding of information in the nervous system
  publication-title: Proc R Soc London Ser B Biol Sci
  doi: 10.1098/rspb.1999.0736
– volume: 17
  start-page: 9315
  issue: 23
  year: 1997
  ident: pcbi.1009832.ref048
  article-title: Interaction between the Postsubiculum and Anterior Thalamus in the Generation of Head Direction Cell Activity
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.17-23-09315.1997
– volume: 7
  start-page: 1
  year: 2016
  ident: pcbi.1009832.ref057
  article-title: Temporal pairwise spike correlations fully capture single-neuron information.
  publication-title: Nat Commun
  doi: 10.1038/ncomms13805
– volume: 17
  start-page: e1008927
  issue: 6
  year: 2021
  ident: pcbi.1009832.ref040
  article-title: Embedding optimization reveals long-lasting history dependence in neural spiking activity.
  publication-title: PLOS Comput Biol.
  doi: 10.1371/journal.pcbi.1008927
– volume: 562
  start-page: 124
  issue: 7725
  year: 2018
  ident: pcbi.1009832.ref053
  article-title: Coherent encoding of subjective spatial position in visual cortex and hippocampus
  publication-title: Nature
  doi: 10.1038/s41586-018-0516-1
– volume: 34
  start-page: 1067
  issue: 3
  year: 2014
  ident: pcbi.1009832.ref039
  article-title: Encoding of head direction by hippocampal place cells in bats
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.5393-12.2014
– volume: 28
  start-page: 13448
  issue: 50
  year: 2008
  ident: pcbi.1009832.ref036
  article-title: Hippocampal network dynamics constrain the time lag between pyramidal cells across modified environments
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.3824-08.2008
– start-page: 800102
  year: 2019
  ident: pcbi.1009832.ref047
  article-title: On the correspondence of electrical and optical physiology in in vivo population-scale two-photon calcium imaging
  publication-title: bioRxiv
– volume-title: Spikes: exploring the neural code
  year: 1999
  ident: pcbi.1009832.ref006
– volume: 41
  start-page: 307
  issue: 2
  year: 2021
  ident: pcbi.1009832.ref025
  article-title: Spatial Information Encoding across Multiple Neocortical Regions Depends on an Intact Hippocampus
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.1788-20.2020
– volume: 440
  start-page: 1007
  issue: 7087
  year: 2006
  ident: pcbi.1009832.ref055
  article-title: Weak pairwise correlations imply strongly correlated network states in a neural population
  publication-title: Nature
  doi: 10.1038/nature04701
– volume: 23
  start-page: 138
  issue: 1
  year: 2020
  ident: pcbi.1009832.ref042
  article-title: A large-scale standardized physiological survey reveals functional organization of the mouse visual cortex
  publication-title: Nat Neurosci
  doi: 10.1038/s41593-019-0550-9
– volume: 4
  start-page: 410
  issue: 4
  year: 1994
  ident: pcbi.1009832.ref015
  article-title: Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input.
  publication-title: Hippocampus.
  doi: 10.1002/hipo.450040404
– volume: 36
  start-page: 1547
  issue: 5
  year: 2016
  ident: pcbi.1009832.ref051
  article-title: Nonspatial Sequence Coding in CA1 Neurons.
– volume: 5
  start-page: 69
  issue: OCTOBER
  year: 2011
  ident: pcbi.1009832.ref022
  article-title: Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex.
  publication-title: Front Behav Neurosci.
– volume: 328
  start-page: 1576
  issue: 5985
  year: 2010
  ident: pcbi.1009832.ref038
  article-title: Development of the Spatial Representation System in the Rat
  publication-title: Science
  doi: 10.1126/science.1188210
– volume: 28
  start-page: 14271
  issue: 52
  year: 2008
  ident: pcbi.1009832.ref044
  article-title: Network dynamics underlying the formation of sparse, informative representations in the hippocampus
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.4261-08.2008
– volume: 10
  start-page: 1731
  issue: 7
  year: 1998
  ident: pcbi.1009832.ref005
  article-title: Mutual Information, Fisher Information, and Population Coding.
  publication-title: Neural Comput.
  doi: 10.1162/089976698300017115
– volume: 7
  start-page: 1
  year: 2018
  ident: pcbi.1009832.ref035
  article-title: Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data
  publication-title: Elife
  doi: 10.7554/eLife.28728
– volume: 46
  start-page: 493
  issue: 3
  year: 2005
  ident: pcbi.1009832.ref008
  article-title: Redundancy in the population code of the retina
  publication-title: Neuron
  doi: 10.1016/j.neuron.2005.03.026
– volume: 14
  start-page: 405
  issue: 2
  year: 2002
  ident: pcbi.1009832.ref027
  article-title: Measuring information spatial densities.
  publication-title: Neural Comput
  doi: 10.1162/08997660252741176
– volume: 65
  start-page: 305
  issue: 5
  year: 1991
  ident: pcbi.1009832.ref012
  article-title: Unbiased measures of transmitted information and channel capacity from multivariate neuronal data.
  publication-title: Biol Cybern
  doi: 10.1007/BF00216963
– volume: 107
  start-page: 703
  issue: 4
  year: 2020
  ident: pcbi.1009832.ref026
  article-title: A Distributed Neural Code in the Dentate Gyrus and in CA1
  publication-title: Neuron
  doi: 10.1016/j.neuron.2020.05.022
– volume: 7
  start-page: 87
  issue: 1
  year: 1996
  ident: pcbi.1009832.ref041
  article-title: Analytical estimates of limited sampling biases in different information measures
  publication-title: Netw Comput Neural Syst
  doi: 10.1080/0954898X.1996.11978656
– volume: 7
  start-page: 365
  issue: 2
  year: 1996
  ident: pcbi.1009832.ref016
  article-title: Speed, noise, information and the graded nature of neuronal responses
  publication-title: Netw Comput Neural Syst
  doi: 10.1088/0954-898X_7_2_018
– volume: 38
  start-page: 305
  issue: 2
  year: 2003
  ident: pcbi.1009832.ref046
  article-title: Hippocampal CA3 NMDA Receptors Are Crucial for Memory Acquisition of One-Time Experience
  publication-title: Neuron
  doi: 10.1016/S0896-6273(03)00165-X
– start-page: 1
  year: 2021
  ident: pcbi.1009832.ref043
  article-title: Representational drift in the mouse visual cortex
  publication-title: Curr Biol
– volume: 23
  start-page: 11539
  issue: 37
  year: 2003
  ident: pcbi.1009832.ref054
  article-title: Synergy, Redundancy, and Independence in Population Codes
  publication-title: Revisited. J Neurosci
  doi: 10.1523/JNEUROSCI.23-37-11539.2003
– volume: 94
  start-page: 83
  issue: 1
  year: 2017
  ident: pcbi.1009832.ref052
  article-title: Grid and Nongrid Cells in Medial Entorhinal Cortex Represent Spatial Location and Environmental Features with Complementary Coding Schemes
  publication-title: Neuron
  doi: 10.1016/j.neuron.2017.03.004
– volume: 27
  start-page: 7854
  issue: 29
  year: 2007
  ident: pcbi.1009832.ref045
  article-title: Experience-dependent increase in CA1 place cell spatial information, but not spatial reproducibility, is dependent on the autophosphorylation of the α-isoform of the calcium/calmodulin-dependent protein kinase II
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.1704-07.2007
– volume: 57
  start-page: 162
  issue: 1
  year: 1987
  ident: pcbi.1009832.ref009
  article-title: Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis
  publication-title: J Neurophysiol
  doi: 10.1152/jn.1987.57.1.162
– volume: 87
  start-page: 1078
  issue: 5
  year: 2015
  ident: pcbi.1009832.ref018
  article-title: Topography of place maps along the CA3-to-CA2 axis of the hippocampus
  publication-title: Neuron
  doi: 10.1016/j.neuron.2015.07.007
– volume: 17
  start-page: 223
  issue: 2
  year: 2011
  ident: pcbi.1009832.ref058
  article-title: Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy
  publication-title: Nat Med
  doi: 10.1038/nm.2292
– volume: 89
  start-page: 299
  issue: 2
  year: 2016
  ident: pcbi.1009832.ref060
  article-title: Simultaneous Denoising, Deconvolution, and Demixing of Calcium Imaging Data
  publication-title: Neuron
  doi: 10.1016/j.neuron.2015.11.037
– volume: 21
  start-page: 1102
  issue: 4
  year: 2017
  ident: pcbi.1009832.ref004
  article-title: Tracking the same neurons across multiple days in Ca2+ imaging data
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2017.10.013
– volume: 328
  start-page: 1573
  issue: 5985
  year: 2010
  ident: pcbi.1009832.ref037
  article-title: Development of the Hippocampal Cognitive Map in Preweanling Rats
  publication-title: Science
  doi: 10.1126/science.1188224
– volume: 7
  start-page: 399
  issue: 2
  year: 1995
  ident: pcbi.1009832.ref011
  article-title: The Upward Bias in Measures of Information Derived from Limited Data Samples.
  publication-title: Neural Comput.
  doi: 10.1162/neco.1995.7.2.399
– volume: 30
  start-page: 1467
  issue: 8
  year: 2020
  ident: pcbi.1009832.ref019
  article-title: Multiple Maps of the Same Spatial Context Can Stably Coexist in the Mouse Hippocampus
  publication-title: Curr Biol
  doi: 10.1016/j.cub.2020.02.018
– start-page: 1
  year: 2002
  ident: pcbi.1009832.ref034
  article-title: Entropy and inference, revisited.
  publication-title: Adv Neural Inf Process Syst
– volume: 361
  start-page: 392
  issue: 6400
  year: 2018
  ident: pcbi.1009832.ref024
  article-title: The hippocampal engram maps experience but not place
  publication-title: Science
  doi: 10.1126/science.aat5397
– volume: 4
  start-page: e12247
  year: 2015
  ident: pcbi.1009832.ref059
  article-title: Hippocampal ensemble dynamics timestamp events in long-term memory.
  publication-title: Elife
  doi: 10.7554/eLife.12247
– volume: 66
  start-page: 15
  issue: 5
  year: 2002
  ident: pcbi.1009832.ref032
  article-title: Binless strategies for estimation of information from neural data
  publication-title: Phys Rev E—Stat Physics, Plasmas, Fluids, Relat Interdiscip Top.
– volume: 26
  start-page: 695
  issue: 3
  year: 2000
  ident: pcbi.1009832.ref007
  article-title: De Ruyter Van Steveninck R. Adaptive rescaling maximizes information transmission
  publication-title: Neuron
  doi: 10.1016/S0896-6273(00)81205-2
– volume: 375
  start-page: 62
  year: 2018
  ident: pcbi.1009832.ref017
  article-title: On Information Metrics for Spatial Coding
  publication-title: Neuroscience
  doi: 10.1016/j.neuroscience.2018.01.066
– volume: 499
  start-page: 295
  issue: 7458
  year: 2013
  ident: pcbi.1009832.ref003
  article-title: Ultrasensitive fluorescent proteins for imaging neuronal activity
  publication-title: Nature
  doi: 10.1038/nature12354
– volume: 80
  start-page: 197
  issue: 1
  year: 1998
  ident: pcbi.1009832.ref030
  article-title: Entropy and information in neural spike trains
  publication-title: Phys Rev Lett
  doi: 10.1103/PhysRevLett.80.197
– volume: 16
  start-page: 264
  issue: 3
  year: 2013
  ident: pcbi.1009832.ref001
  article-title: Long-term dynamics of CA1 hippocampal place codes
  publication-title: Nat Neurosci
  doi: 10.1038/nn.3329
– volume: 85
  start-page: 190
  issue: 1
  year: 2015
  ident: pcbi.1009832.ref020
  article-title: Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts
  publication-title: Neuron
  doi: 10.1016/j.neuron.2014.12.001
– start-page: 1030
  issue: 1990
  year: 1993
  ident: pcbi.1009832.ref014
  article-title: An Information-Theoretic Approach to Deciphering the Hippocampal Code
  publication-title: Proc IEEE
– volume: 18
  start-page: 9020
  issue: 21
  year: 1998
  ident: pcbi.1009832.ref049
  article-title: Firing Properties of Rat Lateral Mammillary Single Units: Head Direction, Head Pitch, and Angular Head Velocity
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.18-21-09020.1998
– volume: 98
  start-page: 1064
  issue: 3
  year: 2007
  ident: pcbi.1009832.ref010
  article-title: Correcting for the sampling bias problem in spike train information measures
  publication-title: J Neurophysiol
  doi: 10.1152/jn.00559.2007
– volume: 319
  start-page: 1260
  issue: 5867
  year: 2008
  ident: pcbi.1009832.ref023
  article-title: Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning
  publication-title: Science
  doi: 10.1126/science.1151120
– year: 2019
  ident: pcbi.1009832.ref029
  publication-title: Relationship between spiking activity and simultaneously recorded fluorescence signals in transgenic mice expressing GCaMP6
– year: 2020
  ident: pcbi.1009832.ref028
  article-title: The dendritic spatial code: branch-specific place tuning and its experience-dependent decoupling.
  publication-title: bioRxiv
– volume: 8
  start-page: 871
  issue: 10
  year: 2011
  ident: pcbi.1009832.ref002
  article-title: Miniaturized integration of a fluorescence microscope.
  publication-title: Nat Methods.
  doi: 10.1038/nmeth.1694
– volume: 6
  start-page: 149
  issue: 2
  year: 1996
  ident: pcbi.1009832.ref021
  article-title: Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences.
  publication-title: Hippocampus
  doi: 10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K
– volume: 15
  start-page: 1191
  issue: 6
  year: 2003
  ident: pcbi.1009832.ref031
  article-title: Estimation of entropy and mutual information.
  publication-title: Neural Comput.
  doi: 10.1162/089976603321780272
– volume: 71
  start-page: 108
  issue: 2
  year: 1969
  ident: pcbi.1009832.ref013
  article-title: On the bias of information estimates.
  publication-title: Psychol Bull.
  doi: 10.1037/h0026857
SSID ssj0035896
Score 2.4071639
Snippet Applying information theoretic measures to neuronal activity data enables the quantification of neuronal encoding quality. However, when the sample size is...
SourceID plos
doaj
pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e1009832
SubjectTerms Analysis
Bias
Bias (Statistics)
Biology and Life Sciences
Calcium imaging
Calcium ions
Calcium signalling
Coding
Cortex (temporal)
Estimation theory
Hippocampus
Hippocampus - physiology
Humans
Information processing
Information theory
Medicine and Health Sciences
Methods
Neural coding
Neuroimaging
Neurons
Neurons - physiology
Research and Analysis Methods
Social Sciences
Spatial data
Spatial discrimination
Spatial resolution
Statistical methods
Temporal lobe
Visual cortex
SummonAdditionalLinks – databaseName: Biological Science Database
  dbid: M7P
  link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3db9MwELeggLQXvmGBgQJC4imssfPhPKENMcFLNQ2Q-mb5c6tUJV3SIu2_585xAkEDHnhr7Uvr853Pvvjud4S8sa4wSluaUMvAQbGmSqSZy8QZaFSU5cZKX2yiXCz4clmdhhduXQirHGyiN9Sm0fiO_BA2bszzLBh7v7lMsGoU3q6GEho3yS1ESaA-dO90sMQs574-F5bGSUqWLUPqHCvTwyCpdxutVhgpUHFGJ1uTR_Af7fRss2666w6hv8dS_rI5ndz7X7buk7vhWBof9Xr0gNyw9UNypy9UefWInB2vZJe41toYUTn6dMe4cXHAXfVfMeodhgdtcQC8Wq-vYrBYbWdjj5uJf4GJFFiv4jH5dvLx64dPSajGkGgY3TaxzoLzRiXjzqaVMg6cRZNRR6WiGj7BQqeZqVLFpSpTV7i0lNLYeaFB4LDK2RMyq5va7pPY5VLPHTwBqpEpZrhzXKeFzV1KrUxlRNggCKEDVDlWzFgLf_9WgsvST4tA8Ykgvogk41ObHqrjH_THKOORFoG2fUPTnouwbkWa6wLsXI6uFwxVV0wBs5RprhiwwSLyGjVEIJRGjbE653LXdeLzl4U4Kqo8gwPkPPsj0dmE6G0gcg0wq2XIj4ApQ4iuCeU-quPAVCd-KlFEDgY1u7771dgNZgTvhmRtmx3S4JV6zjL49ae9Ro8Tg8keWI8uIuVE1yczN-2pVxceqpxzVrCSPfv7sJ6TPYpZJT4Y_oDMtu3OviC39fftqmtf-jX9A6G4WBY
  priority: 102
  providerName: ProQuest
– databaseName: Public Library of Science (PLoS) Journals Open Access
  dbid: FPL
  link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV3db9MwELeggLQXvmGBgQJC4inQ-BInedwQFUiomgZIe7P8OSpVSdW0k_bfc5e4gUyrEG-pfU7tu_PFp_P9jrF3zgurjeMJd4AOirNVouxUJd5io-aQW6e6YhPFfF6en1enfxzFaxF8KNKPgacfVkYvKKZfoQ7eZnc4CEHO1uz0287yQl5WIqTH7Rs5-vx0KP2DLZ6slk1700Hz-n3Jvz5Aswf_O_WH7H44asbHvW48Yrdc_Zjd64tPXj1hZycL1SZ-7VxMSBt9CmPc-DhgqXY_6SY7Tgfb4gBitVxexWiF1q2LOyxM-gtKjqAaFE_Zz9nnH5--JKHCQmIEwCZx3qFDxhWU3qWVth4dQJtxz5XmBp9w8_LMVqkulS5SL3xaKGXdVBgUIu5ceMYmdVO7Qxb7XJmpxxEo7kyDLb0vTSpc7lPuVKoiBjvGSxPgx6kKxlJ2MbUC3ZCeLZK4JQO3IpYMo1Y9_MY_6E9IpgMtgWd3DSgWGfaiTHMj0Hbl5E7hVE0FGhfLwZQacBkQsbekEZLgMWq6f3Ohtm0rv36fy2NR5RkeCqfZXqKzEdH7QOQbXKxRIecBWUawWyPKQ1K_3aJaiQdVymtGMUXsaKeSN3e_GbrRNFC8R9Wu2RINhclzyPDtz3sNHhhDCRxUYy5ixUi3R5wb99SLXx38eFmCgAJe7J_xS3bAKUuku9x-xCab9da9YnfN5WbRrl93e_Y3XOBEWg
  priority: 102
  providerName: Public Library of Science
Title Bias-free estimation of information content in temporally sparse neuronal activity
URI https://www.ncbi.nlm.nih.gov/pubmed/35148310
https://www.proquest.com/docview/2640120633
https://www.proquest.com/docview/2628295344
https://pubmed.ncbi.nlm.nih.gov/PMC8836373
https://doaj.org/article/15c6040502554b3c93bc0d23c8b3f5a3
http://dx.doi.org/10.1371/journal.pcbi.1009832
Volume 18
WOSCitedRecordID wos001084614100003&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVAON
  databaseName: DOAJ Directory of Open Access Journals
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: DOA
  dateStart: 20050101
  isFulltext: true
  titleUrlDefault: https://www.doaj.org/
  providerName: Directory of Open Access Journals
– providerCode: PRVPQU
  databaseName: Biological Science Database
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: M7P
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/biologicalscijournals
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Computer Science Database
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: K7-
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/compscijour
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Health & Medical Collection
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: 7X7
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: https://search.proquest.com/healthcomplete
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: ProQuest advanced technologies & aerospace journals
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: P5Z
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: https://search.proquest.com/hightechjournals
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: ProQuest Central
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: BENPR
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: https://www.proquest.com/central
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Publicly Available Content Database
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: PIMPY
  dateStart: 20050601
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/publiccontent
  providerName: ProQuest
– providerCode: PRVATS
  databaseName: Public Library of Science (PLoS) Journals Open Access
  customDbUrl:
  eissn: 1553-7358
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0035896
  issn: 1553-7358
  databaseCode: FPL
  dateStart: 20050101
  isFulltext: true
  titleUrlDefault: http://www.plos.org/publications/
  providerName: Public Library of Science
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3di9QwEA-6Kvgift5Vz6WK4FO9Nmmb9PFWbvFQl7IqrL6UNB-6sLTLdle4_96ZNLtc5eRefAk0mbbkN5M0aWZ-Q8gbY3NdK0MjahhsUIwuIqljGVkNlTVlmTbSJZvgs5lYLIrySqov9Anr6YF74E6TTOVgaBmufdOaqYLVKtaUKVEzm0nH8xnzYr-Z6udglgmXmQuT4kScpQsfNMd4cup19G6t6iX6CBSC0cFHyXH3H2bo0XrVdtctP__2orzyWZo-JA_8ejI86_vxiNwyzWNyr88wefmEzCdL2UV2Y0yIdBp9nGLY2tATprpLdFeHp0Nd6JmqVqvLEKaaTWdCR3iJr8AICEw08ZR8m55_ff8h8mkUIpUzto2MNbDropIJa5Ki1hZ2eTqllsqaApT4a42mukhqIWue2NwmXEpt4lyBpmB4smdk1LSNOSYhAK5iC3eATkEZWlgrVJKbzCbUyEQGhO1xrJTnGMdUF6vKHZxx2Gv0sFSIfuXRD0h0uGvdc2zcID9BFR1kkSHbVYDdVN5uqpvsJiCvUcEVcmA06GTzU-66rrr4MqvO8iJLYeUXp_8Umg-E3noh20JnlfSBDQAZcmsNJI_Rmvad6ipYjWLwMqgpICd7C7u--dWhGcY_HurIxrQ7lMGz8Iyl8PSj3iAPwGCUBiaSCwgfmOoAuWFLs_zlOMaFYDnj7Pn_gPoFuU8xaMT5up-Q0XazMy_JXfV7u-w2Y3KbL7grxZjcmZzPyvnYDWYop-UnKD_yaIw-uSWUZfYDpMqLz-X3P8MoUjw
linkProvider Directory of Open Access Journals
linkToHtml http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V1LbxMxELZKAMGFNzRQYEEgTqZZex_eA0ItUDVqiVBppdyM148SKdoN2QSUP8VvZGbXG1hU4NQDt8Qebzyzn8eeeB6EPLMuMbm2jDLLwUCxJqPKDBR1BhpzxmNjVV1sIh2NxHicfdgg39tYGHSrbHVirahNqfE_8m3YuDHOM-H89ewLxapReLvaltBoYHFgV9_AZKteDd_C-33O2N674zf71FcVoBoGL6h1FowQprhwNsxy48DoMRFzTOVMwycALItMFuZC5WnoEhemShk7SDRMHNDK4bkXyMWIixTX1UFKW83PY1HXA8NSPDTl0diH6vE03PbIeDnT-QQ9EzLBWWcrrCsGrPeF3mxaVmcden_33fxlM9y7_r-J8Qa55o_dwU6zTm6SDVvcIpebQpyr2-Rod6Iq6ubWBph1pAnnDEoX-Lyy9Vf06gdxQFvgE3pNp6sANPK8skGdFxR_AgNFsB7HHXJyLgzdJb2iLOwmCVys9MDBCIB-lHMjnBM6TGzsQmZVqPqEty9eap-KHSuCTGV9v5iCSdaIRSJcpIdLn9D1qFmTiuQf9LuIqTUtJhKvG8r5qfR6SYaxTkCPx2hawlR1xnNglnEtcg5s8D55ioiUmCqkQF-kU7WsKjn8OJI7SRZHcEAeRH8kOuoQvfBErgRmtfLxHyAyTEHWodxE-LdMVfInaPtkq4X12d1P1t2gJvHuSxW2XCINugzEPIKn32tW0FowGMyC9fb6JO2srY7kuj3F5HOdil0InvCU3__7tB6TK_vH7w_l4XB08IBcZRhBUzv-b5HeYr60D8kl_XUxqeaPan0SkE_nvfJ-AEY6teo
linkToPdf http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V1Lj9MwELaW8hAX3rCFBQICcQpt7DwPCO2yVFSLqmoBqeJiHD-WSlVSkhbUv8avY8ZxCkELnPbArbUnj5l-M_bU8yDkiTaxyqWmPtUMHBStMl-oofCNgsGcskhpYZtNJJNJOptl0x3yvc2FwbDK1iZaQ61Kif-RD2DhxjzPmLGBcWER08PRy-UXHztI4Ulr206jgciR3nwD961-MT6E3_oppaPX71-98V2HAV_CjVa-NhocEipYanSQ5cqAA6RCaqjIqYRPAF4aqizIU5EngYlNkAih9DCWwAQgl8F9z5HzCfiYGE44jT62qwCLUtsbDNvy-AkLZy5tjyXBwKHk-VLmc4xSyFJGO8ui7R6wXSN6y0VZn7YB_j2O85eFcXT1fxbpNXLFbce9_UZ_rpMdXdwgF5sGnZub5PhgLmrfVFp7WI2kSfP0SuO5erP2K0b7g2hgzHOFvhaLjQeWuqq1Z-uF4iMwgQT7dNwiH86EodukV5SF3iWeiYQcGrgCVCLMmUqNSWUQ68gEVItA9AlrQcClK9GOnUIW3J47JuCqNWLhCB3uoNMn_vaqZVOi5B_0B4ivLS0WGLcDZXXCnb3iQSRjsO8RupzwqjJjOTBLmUxzBmywPnmM6ORYQqRA5JyIdV3z8bsJ3wdlCGHjPAz_SHTcIXrmiEwJzErh8kJAZFiarEO5i6rQMlXznwDuk70W4qdPP9pOg_nEMzFR6HKNNBhKELEQ7n6n0aatYDDJBfvw9UnS0bOO5LozxfyzLdGepixmCbv799d6SC6BwvG348nRPXKZYmKNzQfYI71Vtdb3yQX5dTWvqwfWtHjk01kr3g8gIL8O
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Bias-free+estimation+of+information+content+in+temporally+sparse+neuronal+activity&rft.jtitle=PLoS+computational+biology&rft.au=Sheintuch%2C+Liron&rft.au=Rubin%2C+Alon&rft.au=Ziv%2C+Yaniv&rft.date=2022-02-01&rft.issn=1553-7358&rft.eissn=1553-7358&rft.volume=18&rft.issue=2&rft.spage=e1009832&rft_id=info:doi/10.1371%2Fjournal.pcbi.1009832&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7358&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7358&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7358&client=summon